Abstract

Oscillations in network activity are ubiquitous in the brain and are involved in diverse cognitive functions. Oscillation characteristics, such as power, frequency, and temporal structure, depend on both network connectivity and intrinsic cellular properties, such as ion channel composition. An important class of channels, with key roles in regulating cell excitability, are h-channels. The h-current (Ih) is a slow, hyperpolarization-activated, depolarizing current that contributes to neuronal resonance and membrane potential. The impact of Ih on network oscillations, however, remains poorly understood. To elucidate the network effects of Ih, we used a computational model of a generic oscillatory neuronal network consisting of inhibitory and excitatory cells that were externally driven by excitatory action potentials and sustained depolarizing currents. We found that Ih increased the oscillation frequency and, in combination with external action potentials, representing input from areas outside the network, strongly decreased the synchrony of firing. As a consequence, the oscillation power and the duration of episodes during which the network exhibited high-amplitude oscillations were greatly reduced in the presence of Ih. Our results suggest that modulation of Ih or impaired expression of h-channels, as observed in epilepsy, could, by affecting oscillation dynamics, markedly alter network-level activity and potentially influence oscillation-dependent cognitive processes such as learning, memory and attention.

Highlights

  • Using a computational model of a generic neuronal network, we here studied the impact of Ih on network oscillations generated by interacting excitatory and inhibitory cells

  • We looked at the influence of Ih on the occurrence of alternating high-amplitude (HAEs) and low-amplitude episodes (LAEs) in oscillations

  • In our previous work (Avella Gonzalez et al, 2012), we found that the minimal stimulation condition for obtaining high-amplitude episodes (HAEs)-LAE dynamics is a constant depolarizing current (CDC, FIGURE 8 | The effect of Ih on high amplitude episodes (HAEs), frequency, and power of network oscillations diminishes when h-channel conductance is reduced

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Summary

Introduction

Oscillations in electrical activity are a hallmark of many brain networks (Gray et al, 1989; Fisahn et al, 1998; Csicsvari et al, 2003; van Aerde et al, 2008) and are associated with various cognitive functions, such as attention (Fries et al, 2001; Dehaene and Changeux, 2005; Buia and Tiesinga, 2006), temporal binding (Gray et al, 1989; Engel et al, 1999, 2001), learning (Miltner et al, 1999; Caplan et al, 2001), working memory (Raffone and Wolters, 2001; Howard et al, 2003; Haenschel et al, 2009), and memory consolidation (Axmacher et al, 2006). As measured in EEG and extracellular field recordings, are produced by the rhythmic and synchronized firing of large numbers of cells (Buzsaki and Draguhn, 2004; Börgers et al, 2005; Womelsdorf and Fries, 2007) and are thought to arise from interacting populations of excitatory and inhibitory neurons (Tiesinga et al, 2001; Börgers and Kopell, 2005; Börgers et al, 2005). The amplitude (or power) of ongoing oscillations often fluctuates strongly, with high-amplitude episodes (HAEs) alternating erratically with low-amplitude episodes (LAEs; Poil et al, 2008, 2011; Montez et al, 2009; van Aerde et al, 2009; Freyer et al, 2011). Changes in the temporal pattern of amplitude fluctuations have been observed in Alzheimer’s disease (Montez et al, 2006) and ADHD (Dockstader et al, 2008)

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